BTH-Induced Resistance in Rice Impairs Magnaporthe oryzae Metabolic Fitness and Suppresses Key Virulence Genes

Induced resistance primes host immunity for enhanced protection; however, how pathogens respond to this primed state remains poorly understood. Here, we investigated the molecular responses of the rice blast fungus Magnaporthe oryzae during infection of benzothiadiazole (BTH)-primed rice. Seed priming with BTH conferred long-lasting resistance against M. oryzae at the four-leaf stage. Time-course transcriptomic analyses (12–48 hpi) identified 699 differentially expressed genes (DEGs) in M. oryzae, revealing a distinct temporal transition during infection of BTH-primed rice. The fungal transcriptional response shifted from early growth and environmental sensing to enhanced protein turnover, metabolic repression, energy depletion, and genomic instability, indicating progressive impairment of fungal fitness by host immunity. From these DEGs, eight BTH-suppressed candidate virulence genes (MoBVG1–8) were selected for functional characterization. Gene overexpression analyses showed that two genes, MoBVG2 and MoBVG6, significantly increased pathogenicity on BTH-primed rice, while knockout analyses confirmed that both are required for full pathogenicity on non-primed control plants. MoBVG2 encodes a reactive oxygen species (ROS)-scavenging effector, and MoBVG6 encodes an environmental sensor, highlighting the importance of ROS detoxification and environmental perception for successful host colonization. Functional analyses further revealed that MoBVG2 contribute to vegetative growth, while MoBVG6 is required for proper appressorium development. Together, these findings suggest that BTH-induced resistance restricts blast disease by impairing fungal metabolic fitness and suppressing key virulence genes, providing novel insights into the pathogen-side molecular mechanisms underlying chemically induced resistance in plants.